REVIEW published: 17 November 2015 doi: 10.3389/fnmol.2015.00067

Protein and Signaling Networks in Vertebrate Photoreceptor Cells

Karl-Wilhelm Koch 1* and Daniele Dell’Orco 2

1 Department of Neurosciences, Biochemistry Group, University of Oldenburg, Oldenburg, Germany, 2 Department of Neurological, Biomedical and Movement Sciences, Section of Biological Chemistry and Center for BioMedical Computing (CBMC), University of Verona, Verona, Italy

Vertebrate photoreceptor cells are exquisite light detectors operating under very dim and bright illumination. The photoexcitation and adaptation machinery in photoreceptor cells consists of protein complexes that can form highly ordered supramolecular structures and control the homeostasis and mutual dependence of the secondary 2 messengers cyclic guanosine monophosphate (cGMP) and Ca +. The visual pigment in rod photoreceptors, the G protein-coupled receptor rhodopsin is organized in tracks of dimers thereby providing a signaling platform for the dynamic scaffolding of the G protein transducin. Illuminated rhodopsin is turned off by phosphorylation catalyzed by 2 rhodopsin kinase (GRK1) under control of Ca +-recoverin. The GRK1 protein complex partly assembles in lipid raft structures, where shutting off rhodopsin seems to be more effective. Re-synthesis of cGMP is another crucial step in the recovery of the photoresponse after illumination. It is catalyzed by membrane bound sensory guanylate 2 cyclases (GCs) and is regulated by specific neuronal Ca +-sensor proteins called guanylate cyclase-activating proteins (GCAPs). At least one GC (ROS-GC1) was shown to be part of a multiprotein complex having strong interactions with the cytoskeleton and 2 being controlled in a multimodal Ca +-dependent fashion. The final target of the cGMP signaling cascade is a cyclic nucleotide-gated (CNG) channel that is a hetero-oligomeric Edited by: protein located in the plasma membrane and interacting with accessory proteins in highly Jean-Marc Taymans, UMR1172, Jean-Pierre Aubert organized microdomains. We summarize results and interpretations of findings related to Research Center, France the inhomogeneous organization of signaling units in photoreceptor outer segments. Reviewed by: Alexander Dizhoor, Keywords: multi-protein complexes, second messenger signaling, phototransduction, cGMP, calcium-binding Salus University, USA proteins Johann Helmut Brandstätter, FAU Erlangen-Nuremberg, Germany INTRODUCTION *Correspondence: Karl-Wilhelm Koch Vertebrate photoreceptor cells are neurosensory cells of unique morphology and specialized [email protected] function. They are divided into two general types, rods and cones, which mediate vision at night and daylight, respectively. Absorption of photons by visual pigments, rhodopsin in Received: 25 September 2015 rods and cone opsins in cones, triggers a well understood signaling cascade that has been Accepted: 26 October 2015 thoroughly investigated in the past decades. Numerous articles in the last decades have therefore Published: 17 November 2015 summarized the basic features of the phototransduction process (e.g., Stryer, 1991; Kaupp and Citation: Koch, 1992; Koch, 1994; Pugh and Lamb, 2000; Luo et al., 2008; Wensel, 2008; Arshavsky Koch K-W and Dell’Orco D (2015) and Burns, 2012; Korenbrot, 2012; Palczewski, 2012): coupling of visual pigments to the Protein and Signaling Networks in heterotrimeric G protein tra